The presence of wild edible plants and determinants influencing their harvest, consumption, and conservation in south eastern Bhutan

Definition Wild edible plants (WEPs) grow naturally in self-maintaining ecosystems. WEPs are harvested for consumption, sale, and medicinal uses. We hypothesize that WEPs play a major role in supplying food and generating income for the rural people in a world that is increasingly recognising its emerging conservation issues. We tested this hypothesis by identifying the reasons for harvest, consumption, and conservation of WEPs using focus group discussion, field observations and questionnaire surveys in south eastern Bhutan in late 2019. Methods Focused group discussions were held with the local people to identify reasons for harvest and consumption of WEPs. Data on the identified reasons for harvest, consumption, and conserving WEPs were determined using a questionnaire survey with ranking scales for a set of 76 randomly selected households. Representative field-observations and questionnaire surveys were carried out in villages close to forests. Parts of the plant used, how these were consumed, harvest season, and plant (life form) were recorded. The data was subjected to a Kruskal-Wallis rank sum test and weighted averages calculated. Result and conclusion A total of 120 WEPs belonging to 63 families (including Agaricaceae) were reported. Most of the WEPs recorded were trees (45.0%) then herbs (25.8%), vines (13.3%) and shrubs (10.8%). The commonly consumed plant parts were the fruit (43.3%), shoots (28.3%) and leaves (20.8%). The purposes for harvesting and consumption, conservation of WEPs were significantly (P<0.001) different, while the motivations for collecting WEPs were not. The motivation for collecting WEPs were family consumption > sale > medicinal uses > preservation for future use > insufficient food from cultivated source’s. The two most important strategies for conservation were to domesticate the WEPs and cultivate in forests. The findings reveal valuable lessons and insights about the reasons for harvesting, collection, consumption, and conservation of WEPs.


Background
Forests represent a crucial resource stock for local people [1].They supply a diverse array of foods, vegetables, medicines, firewood, timber, handicraft materials, etc. to communities [2,3].Wild Edible Plants (WEPs) are plant species that are harvested for human consumption: they are critical for inclusive world food security [4].Wild Edible Plants are defined as plants which grow naturally among self-maintaining populations in natural or semi-natural ecosystems and can exist independent of direct human action [5,6].
Humans have been using forests intensively since the dawn of civilization and this has often resulted in the wise management of forest resources [6].These people harvest WEPs for selfconsumption, and to meet supply of an array of livelihood commodities [7][8][9].WEPs provide important nutrients and bioactive compounds in traditional diets which offer valuable health benefits [10].There is a positive correlation between poverty and reliance on Non-Timber Forest Products [11] and WEP consumption and food security of local communities [12].There is also a positive correlation between humans and their genes with diets derived from the environment; some claim that contemporary diets and lifestyles devoid of these diets underlie many of the chronic health problems of humans today [13].Further, human malnutrition often coexists with lifestyle diseases such as overweight/obesity [14] often due to these socioeconomic-environmental changes.Changes in traditional landscapes, cultures, and food chains compel communities towards adverse nutritional transitions affecting human health negatively [15].In addition, consumption of highly-processed foods negatively affects human health and leads to undesirable outcomes such as gut inflammation [16].

WEPs have food, nutritional and medicinal value
Approximately two billion people globally experience hunger due to lack of nutrition [17] and WEPs have the potential to help address the food security [18].Numerous WEP species in any particular area are traditionally used as vegetables to supply nutrition and boost food security of the local communities [18,19].WEPs are cheap and highly suitable alternative sources of healthy and nutritious foods and are vitally important for supporting the global food basket in general, particularly in sub-Saharan Africa [20].In the face of changing environments, and food dynamics due to market chain disruptions and globalization, current food systems are waning in their ability to deliver a healthy diet [21].Age-old traditional diets are recognized in offering prized health benefits [10] because WEPs form vital dietary sources to the rural poor [22,23].Moreover, dishes prepared from WEPs have become special delicacies even in the menu of urbanites [24].Dependency on WEPs for the supply of food is still common among rural communities of developing [25] and developed countries [26].
Many indigenous populations have relied on wild products for aeons in order to eat a balanced diet particularly during times of critical food shortages [9,27,28].In their review of literature, Pinela et al [29] highlighted the importance of the role of WEPs in supplying important nutrients.Some WEPs contain a minimum daily intake amounts of essential nutrients [30].Traditional foods are richer in micronutrients than conventional cultivated foods [31], and perfectly complement a diet supplied by conventionally cultivated crops.WEPs supply bioactive compounds/functional foods which can contribute to healthy diets that boost immunity helping to protect against an array of illnesses [30,32].A correlational study on WEPs and diets conducted in a traditional community in Indonesia found that anaemic conditions among pregnant women are associated with a deficiency of vegetables and fruits in daily diets sourced from conventionally cultivated crops [33].The abundance of many WEPs could help improve this situation [34].WEP foods present a viable alternative option for alleviating micronutrient deficiency among rural and indigenous people [35].Further, in a comparative study, WEP consumers had a significantly higher intake of Vitamins A, B6, and C, and calcium [36].Despite the huge potential of WEPs to supply myriad of nutrients to the consumers, WEPs are not recognized as a noteworthy contributor to the food basket, particularly in the developed countries [37].Besides dietary nutrients, many WEPs also have medicinal properties [38,39].Diverse wild plants consumed in India are also reported to have a range of medicinal uses [3].In Bhutan, this bi-dimensional use of WEPs is commonly reported, for example by Wangyal [40], Zangpo, Tshering [41], and Dema and Dolkar [42].A study in Tibetan plateau reported the use of thirtyone WEP species as medicines to treat gastropathy, coughs, fevers, rheumatism, dysentery, fractures, dyspepsia, hemoptysis, and asthma, in addition to their use as special tonics [43].

WEPs have traditional and economic value
Traditional knowledge of WEPs is associated with indigenous food systems [44].Culinary preparations of certain WEPs are often delicacies and are consumed during major festivals [3].Similarly, WEPs are associated with local festivals, rituals and funerals in Khoma, a village in the Lhuentse district in Bhutan [42].Likewise, varieties of wild Dioscorea species are harvested and consumed in special preparations during Losar (New Year), Lochoe (an annual ritual) and Prechula (an offering to local deities) in the Kheng region of central Bhutan [28].Valuable indigenous knowledge on the preparation and use of many traditional dishes is being lost over time, triggered by rural to urban lifestyle changes [45].
The decline in the availability of WEPs also diminishes the valuable traditional knowledge pertaining to diverse use of WEPs [36].A study from Khaling in the Trashigang district in eastern Bhutan on forest ecosystem services availed by the locals showed that Nu. 21.6 million (1 USD � Nu.76) worth of forest commodities are produced annually [46].

The conservation of WEPs
The potential loss of some WEPs is of global conservation concern.Species has been for example Psilotrichum axilliflorum is listed as endangered, and Mitragyna stipulosa and Vitellaria paradoxa are listed as vulnerable [39].Unregulated and over-exploitation of forest resources results in disharmony between forest resource consumers [50].Declines in species density and biodiversity richness in the natural habitat occur [24,62].
There is a widespread ignorance about the loss of WEPs diversity and decline in abundance at policy level [e.g.63,64].A recent review by Bajgai [50] showed a lack of clear quantification of the food and nutritional benefits supplied by WEPs: this resulted in the potential benefits of WEPs being overlooked and omitted from mainstream developmental programs [6,19].These omissions could have been driven by a compulsion to produce cash crops and starchy staples [65] that have featured strongly in governmental development agenda.Additionally, a severe lack of nutrient composition data results in limited quantification of the benefits of WEP, and their dietary contribution [35,50].In contrast, unrestricted access to WEPs may have resulted in oversupply and a lowering of commercial value in the past, further reducing WEP prominence image [66].Since it is quite unrealistic to single out any particular harvesting method as sustainable [67], developing agro-techniques for the mass production of WEPs for conservation and for meeting the nutritional and livelihood needs of indigenous communities [3,5,19].Alarmingly, WEPs are under constant threat from habitat destruction from anthropogenic (livestock grazing, agricultural land expansion and over-exploitation of WEPs) and natural phenomena (forest fire, and climate change), which collectively cause indirect loss of valuable traditional knowledge in Bhutan [42].Despite this, there is a general lack of understanding about the role WEPs have in food system and the socio-economy of Bhutanese.We hypothesize that WEPs play a major role in supplying food and generating income for rural people in the face of emerging conservation issues.We tested this hypothesis to identify the purposes for harvesting, consumption, and conservation of WEPs using focus group discussion and field surveys in the villages close to forests in south eastern Bhutan.The study also aims to determine the presence and uses of WEPs species in the study area.A simplified conceptual framework of the study is presented to depict the major steps involved (Fig 1).

Study area
Bhutan lies between the coordinates 26.7263 and 28.2466˚N, and 88.7495 and 92.1236˚E in the eastern Himalayas.It is geographically located between India in the East, West and South, and China in the North.Bhutan is divided into twenty districts.Samdrup Choeling is one of the sub-districts (dungkhag) of Samdrup Jongkhar district and lies between the coordinates of 26.7848 and 27.2473˚N and 90.9981 and 92.1187˚E in south eastern Bhutan.Samdrup Choeling dungkhag is further divided into four administrative areas viz.Samrang, Pemathang, Phuntshothang and Martshala.Samdrup Choeling dungkhag is located 68 km away from the district headquarters of Samdrup Jongkhar.A modern motorable road connects it.Similarly, modern bitumen roads connect each administrative area; and farm roads (unsealed) connect the villages within.There are also government enterprises such as coal mines, fisheries, poultry farming and dairy farming on small and medium scales, and public institutions like schools (primary, lower secondary, middle secondary and higher secondary), health care and Renewable Natural Resources (RNR) centres.Apart from the local inhabitants, there are also public servants; private employees and business people living in the dungkhag.Most importantly, there is a designated area for weekend's market at Tshangchutham village (Phuntshothang).The present study was conducted in the nearby forests surrounding the villages (Khateythang, Mindrupling, Khamethang, Tshangchum, Pemathang, Dungkharling, Chichhosa, Drupchhugang, Zhomlatthang and Majwa) of Samrang, Pemathang, Phuntshothang and Martshala areas.Samdrup Choeling is surrounded by evergreen tropical forest covering the foothills, plateaus, and plain lands.The sub-district has subtropical climatic conditions with annual rainfall of 3582 mm, average monthly minimum temperature of 16.72˚C and average monthly maximum temperature of 25.94˚C [68].Predominantly agrarian, farmers in the study area practice subsistence agriculture.

Qualitative method-focused group discussion
A village nearby a forest was purposively selected in each of the four areas (Geogs) of Samrang, Pemathang, Phuntshothang and Martshala under Samdrup Choeling sub-district where focus group discussions were held in November and December 2019.Members of the focused groups were selected in consultation with heads of villages (Tshogpa) and consisted of those who were aware of the use and knowledgeable of WEPs.Eight to 10 village elderlies of both the genders represented the group in a one-day consultation meeting in the participants' mother tongue to discuss the availability and uses of WEPs in each village.The identified WEPs along with the characteristics of each WEP were recorded.Additionally, the focus group discussions helped formulate the questions for the follow-up questionnaire survey with particular emphasis on identifying the reasons for (a) harvest, (b) collection, (c) consumption, and (d) conservation of WEPs.Five representative attributes or ranks for each of these four major reasons were selected though group discussions and consensus.At the end of each focus group discussion, a key informant was identified to assist in constructing a sampling frame or system for the field survey.

Field survey
Following the focus group discussions, a semi-structured questionnaire field survey was conducted in the Samdrup Choeling sub-district to assess the factors that influence the use and conservation of WEPs.The surveyors were trained prior to the survey to ensure uniformity in execution of the survey conducted between January and October 2020.The identified key informant helped with the sampling frame of the relevant households prior to the implementation of the questionnaire survey.Purposive sampling was used because this method allowed random selection of households without biases [69].A total of 76 randomly selected farmers from the sampling frame were interviewed, which was more than the required 5% sample size recommended for a representative study [70].Prior to an interview, each farmer was briefed and asked for consent and only farmers who consented were included in the focused group discussion and responses to questionnaires.Each set of five questions (attributes/ranks) on the four key aspects of purposes of harvesting, motivations for collection, reasons for consumption, and strategies on conservation of WEPs identified in the focus group discussion were covered in the questionnaire survey.The five attributes/ranks under each of the four major aspects were written in the question response format and were ranked during the interview based on the respondents' priority on a 5-point scale (1 = lowest priority, 2 = low priority, 3 = moderate priority, 4 = high priority and 5 = highest priority) to quantitate the qualitative responses for statistical analysis [71,72].Such scoring is a simple and flexible way of collecting data for a farmer perception study [73,74].
The WEPs identified and listed during focused group discussion were assessed in the wild and in the cultivated/fallow land to ascertain the presence in the sub-district.In other words, a species presence verification was conducted along with the questionnaire survey.Herbarium specimens of unfamiliar plants were collected, later identified using The Flora of Bhutan [75] and other literature [2,[76][77][78], and stored in the Life Science Museum of Sherubtse College, Royal University of Bhutan, Trashigang.Other key information on plant parts used, season of harvest, type of plant (life form), and consumption was also recorded.Post-field survey focused group discussions were held to discuss usage and consumption.Respondents' demographic indicators of gender, age range and literacy level were also captured.The minimum age of a respondent was set at 20 years to ensure that the responses were more reliable.

Statistical analyses
Since the data generated in this study were non-parametric in nature (and not fulfilling the assumptions of an ANOVA), a Kruskal-Wallis test by ranks (equivalent to one-way ANOVA for parametric data) were used for statistical data analyses using the IBM SPSS Statistics (Version 22) predictive analytics software.This methodology is more appropriate to analyse nonparametric or ordinal data [79,80].The data collected on the five attributes/ranks under the major aspects of (a) purposes of harvesting, (b) motivation for collection, (c) reasons for consumption, and (d) strategies on conservation of WEPs were assessed using a boxplot and then subjected to Kruskal-Wallis test by ranks.Significantly, different values were segregated using a Dunn test to make inferences across the attributes.Raw data were processed and computed using Microsoft Excel.Plots were generated using Microsoft Excel and the Statistical Tool for Agriculture Research (STAR version 2.0.1).To substantiate and compare with the inferential statistical analysis, weighted averages were calculated.The responses of the farmers' rankings were organized in descending order and compared.For this, a weighted average, with weights of 1 to 5 were assigned corresponding to the ranking scale of 1 to 5, and then calculated using a simple arithmetic formula (Eq 1) where, X is the weighted average mean, x i is the multiset of data, and w i is the weights (1-5) assigned to each of the data sets.The generated Kruskal-Wallis test by ranks were plotted along with the calculated weighted averages so that comparisons could be made.

Demographic profile of respondents
There were 76 farmers (>20 years of age) who took part in the voluntary questionnaire survey.
In terms of gender representation, 55.3% were male and 44.7% female farmers.Seventy-five per cent of the interviewees were between 20 and 50 years of age while the remainder were > 50 years old.The plurality of the respondents was 36.8% illiterate; few had a diploma/ degree or higher education; while the remaining fell into other categories (non-formal education-11.8%,primary school-13.2%,and high school-30.3%).

Statistical findings
The median, spread and skewedness of the four data sets are graphically demonstrated ( .The nonparametric test of Kruskal-Wallis rank sum test for several dependent samples, which is equivalent to one-way ANOVA for parametric tests, was used to analyze the data were ranks or categorical.Reasons for harvest, consumption, and conservation of WEPs were highly and significantly different (P<0.001),while the motivating factors for collection were not (Table 3).Since the ranking scale used in the study was 5 = highest priority to 1 = lowest priority, a numerically higher mean rank implies a higher priority and vice-versa, therefore the mean ranks or the weighted averages should be elucidated in this context (Figs 3 to 6).

Purposes of harvesting wild edible plants
The data for medicinal uses and sale are symmetrically distributed, whilst that of preserve for future is skewed towards the lower quartile (39% respondents ranked 2 nd rank) (Fig 2A).However, data for family consumption and insufficient food are fully skewed in opposite directions.Family consumption is skewed towards upper extreme value (rank 5) as the median, lower quartile and upper extreme value coincided since 68% of the respondents ranked the purpose 5.
The results of Kruskal-Wallis rank sum test showed that most of the purposes of harvesting WEPs were highly and significantly different (P<0.001) to each other (Fig 3 and Table 3).The highest mean rank was for family consumption (290) since 68% of the respondents ranked it as 5 (Fig 2A), and this was significantly higher than the other four purposes of harvesting WEPs.The lowest rank was for the insufficient food from cultivated sources (133), a result of 53% of respondents categorizing this as rank 1 (Fig 2A ): it was significantly lower compared with the other four purposes of harvesting WEPs, except for preserve for future use.Additionally, the data for insufficient food from cultivated sources is fully skewed towards the lower extreme value and the median coincides with a rank of 1.The weighted averages values show the degree of importance and closely follow the mean ranks.The mean ranks and weighted averages for purposes of collecting WEPs were: family consumption > for sale > medicinal uses > preserve for future use > insufficient food from cultivated sources (Fig 3).

Motivating attributes to collect wild edible plants
Data for good taste, salability and time-efficient are symmetrically distributed (rank 3 as median), while that of availability is slightly skewed towards the upper extreme value even though the median is rank 3 (Fig 2B).However, high price is skewed towards the lower extreme value with rank 2 as the median as 30% of respondents characterized it as rank 5.The statistical results of Kruskal-Wallis rank sum test showed that the motivating factors to collect WEPs were not significant (P = 0.435) to each other even though the mean ranks ranged from  3).Moreover, the weighted averages ranged from 14.3 to 16.4 and closely followed the trend of mean ranks (Fig 4) hence, the null hypothesis of factors being the same is accepted.

Reasons for consuming WEPs
The data for consume differently, easily available and palatability are fairly symmetrically distributed with a median rank of 3.However, for health benefits there is a strong skewedness towards the upper extreme value (median = rank 5) and 64% of the respondents ranked it as 5.
The mean ranks for most of the reasons for consuming WEPs were statistically different (P<0.001) to each other (Fig 5 and Table 3) with health benefits (279) as the highest priority and nutritious (142) as the lowest.This is also indicated by the strong skewedness of data towards rank 5 for health benefits (Fig 2C ) with 64% of the respondents, and the skewedness of nutritious to rank 1 with 36% of the respondents.The mean ranks of palatability, easily available, and consumed in different ways did not differ significantly from each other even  though the mean ranks ranged from 165 to 198 (Fig 5).Additionally, the weighted averages which ranged from 11.9 to 21.1 closely followed the trend in mean ranks.

Strategies to conserve WEPs
The data for decrease harvest and implement regulations are symmetrically distributed (median = rank 3), while those for cultivate in forest and domesticate are skewed towards rank  3) at P<0.001.The two most important strategies to conserve WEPs were to cultivate in farm (or domesticate) and forests as these had significantly (P<0.001) higher mean ranks (�223) compared with the other three strategies (�190); this can be further verified by the graphical data distribution showing skewed data towards rank 5 (median = 4) (Fig 2D).
The least important strategy to conserve WEPs was to stop harvesting (mean rank = 135) and this had a significantly lower mean rank than the other four strategies (Fig 6).Strategies of decreasing frequency of harvest and to implement stringent regulation were of moderate importance and were significantly different to the other three strategies (Fig 2D).Further, the data for stop harvesting is strongly skewed towards rank 1 with 51% of the respondents categorising it as this.Further, the data trend is cross-validated using the weighted averages as they closely follow the mean ranks.

Presence, consumption, plant types and seasonality of WEPs
Bhutan is one of the 10 global hotspots for biodiversity [81].The large number of WEPs species (120 from 63 families) reported (Table 1) is reflective of this, due mainly to the favourable subtropical conditions suitable for a diverse range of plant species.A separate study reported 99 species in 55 plant families from Khoma village of the Lhuntse district in north east Bhutan [42].Similar studies in neighbouring Bangladesh reported 102 WEPs [82], and in Nepal 85 WEPs [2].The number of species reported can vary based of the geographical coverage as a major exploratory study in India reported observing 1403 species belonging to 183 families of WEPs [83]), in contrast to 41 species belonging to 17 families from the Manang district of Nepal [84].A study in Sikkim found 190 species under 78 families [85] which is comparable with our findings.Of 120 species consumed in our study, most were consumed cooked, raw, pickled, chewed or in other forms (Tables 1 and 2).Consumption method is dependent on the type of WEPs and difference are widely documented in literature from around the world [2,3,5,36,38,45,86,87].Similarly, preparation methods depending WEP type including, eaten either cooked or raw, consumed as pickles, decocted as tea, chewed as betel, used for extracting the oil or juice, eaten as nuts by roasting, or even consumed as spices [2,3,5,36,38,45,50,86,87].
The most commonly consumed plant parts in the study were fruits (43.3%), shoots (28.3%) and leaves (20.8%) (Tables 1 and 2).This trend corroborates other studies in the region, for example in the northern Indian state of Uttarakhand [86] and in the Chinese region of Tibet [43].Additionally, our findings match closely with the consumption preference from Bhutan and Nepal [42,88] and are comparable to a study from a reserve park in India [19], i.e., fruit > shoot > leaf.
The WEPs reported in the study were also classified into plant types (Table 1) with most of the WEPs recorded being trees (45.0%), herbs (25.8%), vines (13.3%), and shrubs (10.8%) (Table 2).Recent literature from neighbouring India supports our findings on the composition of plant type [86,87].A major percentage of the WEPs species were harvested in spring and summer, possibly due to favourable seasonal plant growth, however only 14.2% were harvested year-round.Twenty-five per cent of WEPs reported were invasive which presents a concern for the long-term survival of native species [e.g.89].

Purposes of harvesting WEPs
The purposes for harvesting WEPs were significantly different (P<0.001) to each other (Fig 3) with the most important being for family consumption (68% of the respondents ranked it as 5 (Fig 2A )) and the least important being insufficient from the cultivated sources' a trend also reported by others [19].This is because WEPs are known to diversify the family food basket and meet the nutritional requirements of the local people [31].
The median of for sale and medicinal uses was rank 3 (Fig 2A) and they did not differ significantly from each other (Fig 3).This suggests the moderate role played by the WEPs for providing healthy food, and as a means to generate cash income.The lowest median and mean rank were for the insufficient food from cultivated sources indicating that farmers have the potential to be self-sufficient from their farming activities to some extent.In contrast, 64% of the respondents harvested wild Dioscorea species due to the insufficient rice and maize yields from cultivation in Nangkor in the Zhemgang district in central Bhutan in a separate study [28].Further, Dema and Dolkar [42] reported that only 10% of WEP collections were for sale and that 90% were for the domestic consumption because access to markets was limited in that northern central area.The attribute of preserve for future use was also rated significantly lower possibly due to a lack the storage such as deep-freezing facilities or ignorance of modern processing and storage techniques.In other words, lesser quantities of WEP foods were likely to be preserved for consumption in lean seasons.
The relative importance of the purposes for collecting WEPs were family consumption > for sale > medicinal uses > preserve for future use > insufficient food from cultivated sources indicating varying degree of role played by the WEPs in supporting the rural livelihood in general.Moreover, the data of Kruskal-Wallis rank sum test closely match that of the weighted averages across all the analyses confirming the findings.

Motivating attributes to collect WEPs
The common motivating attributes of local people collecting WEPs were assessed by ranking the five questions on salability in the market, time efficiency for collection, availability in the vicinity of the locality, they tasted good, and ability to generate high price.The median, which is a measure of central tendency for a non-parametric analysis, which is same for all five attributes (rank 3) (Fig 2B) except for fetches high price with the median of rank 2, implying a non-significant difference.Although the motivating attributes differed slightly numerically (177 to 209) in terms of by Kruskal-Wallis rank sum test, they did not differ significantly (P = 0.435) (Fig 4) indicating similar priorities or degrees of importance to the respondents.The weighted averages of the motivating attributes (range = 14.3 to 16.4) followed closely with the trend of mean ranks reinforcing the validity of the finding.
In contrast to this study, WEPs collected and sold in Nepal were reported to fetch high prices [2,23]: the differences could be related in contextual variation.In South Africa, the high price of WEPs has been a motivation for the poor households to harvest and sell WEP commodities in the local market [9].Similarly, Namgyel [59] reported that the high price of Cordyceps (a genus of fungi widely used for medicinal purposes) as the motivation to harvest it from localites in the Bhutanese highlands.

Reasons for consuming WEPs
The five most important reasons for consuming WEPs were palatability, nutritious, consumed in different ways, easily available and health benefits or of medicinal value.The mean ranks for the reasons for consuming WEPs were statistically different (Fig 5) with health benefits the highest priority and the nutritious as the lowest.There are important reasons why WEPs should be, and are consumed by the local people, these include the overlapping reasons of use as food and for medicinal value [87].The reasons of palatability, nutritious and consumed in different ways did not differ (had the same median, Fig 2D ), and it can be inferred that these were of similar priority to the respondents.Good taste, and freely available were the two most important perceptions while cultural identity was a negative indicator demonstrated by the indigenous communities in India [19].Since WEPs grow naturally in the wild they are the equivalent of organically produced foods [50,90]), and are nutritious and palatable.Fungo [45] reported that consumption would increase four times if people knew that WEPs foods were more nutritious than foods from a cultivated source.In contrast, our research revealed that local people were aware of the palatable and nutritious values of the WEPs, and that health benefits featured very strongly with 64% of the respondents ranking it as rank of 5 (highest priority) (Fig 2D) even though a majority of farmers (61.8%) had � primary school education.

Strategies to conserve WEPs
An understanding of local people's priority for WEPs conservation strategies were projected from their ranking responses because WEPs are under various constant natural and anthropological threats [43,88].The identified strategies to conserve WEPs were significantly (P<0.001)different (Fig 6 , Table 3), and the two most important strategies were to cultivate in farm or domesticate and cultivate in forests, both of which had a median score of rank 4 (Fig 2D).Thirteen species of WEPs are already domesticated by farmers in north-central Bhutanese district of Lhuentse in congruence to the findings of others [42].According to Bharucha and Pretty [65] people who depend on forest resources maintain resources by the deliberate sowing of wild seeds, burning dried leftovers to stimulate plant growth, leaving portions of roots or replanting material, and extraction of only the required and useful parts while harvesting; these are synonymous to agricultural activities designed to enhance WEPs' productivity.In northern Thailand, rice farmers plant many wild edible plants along irrigation canals, swamps, field boundaries and roadsides [91].Many WEPs are also cultivated in the home gardens, which can become refuges for WEPs threatened by urbanization, drought, and deforestation [92].WEPs such as Artocarpus heterophyllus Lamk., Bauhinia purpurea L., Bauhinia retusa Roxb., Colocasia esculenta (L.) Schott, Emblica officinalis Gaertn., were reported to be domesticated in home gardens in Odisha, in eastern India [87].People who hold primary ownership of WEPs are key stakeholders of WEPs for conservation [59].Hence conservation measures should also be aimed at these people and scaffolded to include their understanding of conservation issues.
Local people consider decrease frequency of harvest and implement of regulation as other prioritised methods (median = rank 3) of conserving WEPs because the high prices in the local markets could stimulate over-harvesting behaviour leading to conservation concerns such as those reported in Nepal [88].Likewise, the decline of Dioscorea in Nangkor Geog under Zhemgang district in south central Bhutan [28] is clear evidence of the negative impact of over-harvesting.Similarly, in Cameroon, a WEP (Gnetum africanum and G. buchholzianum) has been pushed towards vulnerable status due to over exploitation [9].Besides affecting conservation efforts, over exploitation will reduce the availability of WEPs in the long term and thus negatively impact the nutrition security of the local people [65].The least prioritised conservation strategy was to stop harvesting because 51% of the respondents categorized it as rank 1 (median = rank 1).Further, a stop harvesting strategy may be perceived by farmers as a way of deprivation from WEPs collection, and thus negatively affecting their food and nutrition security.Hence, cultivating WEPs in farm and forest contexts are better conservation strategies based on the respondents' opinions.In Bhutan, local people have noticed ecosystem changes and declining trends in the availability of forest resources [46].In response, the government has developed a strategy for the sustainable harvest and conservation policy of non-wood forest products including the WEPs [60,93], which has had a tremendous impact on how we perceive and manage our forest resources [59], even though it may take long time to realise the expected impact.
Most studies have not considered the status on WEPs as native or invasive.In the current study, 25% of 120 species reported were invasive (Table 1), which potentially results in both negative and positive impacts [94,95].Negative impacts include the ability of invasive species to suppress native species and threaten bio-diversity [e.g.89,96], while positive impacts can include harvesting helping to curb invasiveness [2,3,86,97] so long as replanting and futher spread does not occur.Lantana camara L. is an example of invasive WEP reported in Samdrup Choeling [67,87], and previously planted as an ornamental across Bhutan [98].Consuming invasive plants can help bridge food security and garner extra income for the rural people.There are many WEPs which are invasive and some examples are: Tropaeolum majus L., Boerhavia diffusa L., Aconogonon molle (D.Don) H. Hara, Bidens pilosa L., Girardinia diversifolia (Link) Friis, Urtica dioica L., Nasturtium officinale R.Br., Oenanthe javanica (Blume) DC., Adhatoda vasica L., Houttuynia cordata Thunb., Solanum nigrum L., Amaranthus spinosus L., Pteridium aquilinum (L.) Kuhn, Remusatia vivipara (Roxb.)Schott., Elatostema lineolatum J. R.Forst.& G.Forst., Chenopodium album L. and Boehmeria sp Jacq.[77,78,98].Many of these species have not previously been recorded as present in Bhutan and need to be added to an updated National inventory of alien species [98].The presence of these invasive species raises conservation concerns due their ability to suppress native WEPs and to cause a range of other negative impacts.Prompt risk assessment and prioritisation for management would be prudent [99].

Conclusion
The presence of 120 WEPs species belonging to 63 families (including one Agaricaceae) were reported.Most of the WEPs recorded were trees followed by herbs, vines and shrubs, while the commonly consumed plant parts were fruit, shoots and leaves.The relative importance of the purposes of collecting WEPs were family consumption > for sale > medicinal uses > preserve for future use > insufficient food from cultivated sources.There are important reasons why WEPs should be and are consumed by the local people, including the overlapping reasons of food and medicinal value from WEPs.The data revealed that the palatability, nutritious and consumed in different ways categories of WEPs were of similar priority, whereas the health benefits associated with consumption was of the highest priority to the respondents.Two of the most important conservation strategies were to domesticate and cultivate in forests.The data of Kruskal-Wallis rank sum test closely match with that of weighted averages across all the analyses reinforcing the findings.The results reveal a range of valuable understandings and insights into the purposes of harvesting, motivations for collection, reasons for consumption and strategies on conservation of WEPs.

Fig 2 .
Fig 2. Local perceptions around the collection of wild edible plants (WEPs) reported by n = 76 informants in the Samdrup Choeling subdistrict in Bhutan.In a two-stage process, a focus group identified four important aspects of WEP collection (A-purpose of harvest; Bmotivation to harvest; C-reason for consumption; D-strategies for conservation).Informants then ranked each characteristic within the attribute.Data distribution by median, spread and skewedness of the four data sets is illustrated.Characteristics are abbreviated as: Fam_cons = family consumption, Insuff_food = insufficient food from cultivated sources, Medicinal = medicinal uses, Preserve = preserve for future use, Sale = for sale, Timeeffic = time efficient, Cons diff = consume in different ways, Easi_Avai = Easily Available, Health_B = health benefits, Cul_Fores = cultivate in forest, Dec_harv = decrease harvesting, Domesticate = cultivate in farm, Imple_law = Implement regulations and stop harv = stop harvesting.https://doi.org/10.1371/journal.pone.0285936.g002

Table 1 . Wild edible plants documented from the study sites and reported by focus groups of n = 8-10 expert elder participants from four areas-Samrang, Pemathang, Phuntshothang and Martshala in south eastern Bhutan.
Plants are arranged alphabetically by local name.

Table 3 . Summary of Kruskal-Wallis rank sum test for several dependent samples
. Kruskal-Wallis rank sum test showing consensus on local prioritization of purposes for harvesting wild edible plants (with family consumption highest, see Fig 3); reasons for consuming (with health benefits highest, see Fig 5); and strategies for conservation (with cultivation/domestication in farm / in forest highest, see Fig 6); but not for motivating attributes of collection (no significant difference, see Fig 4).